SIV infection and ARV treatment reshape the transcriptional and epigenetic profile of naïve and memory T cells in vivo

J Virol. 2024 Jun 13;98(6):e0028324. doi: 10.1128/jvi.00283-24. Epub 2024 May 23.

Abstract

Human and simian immunodeficiency viruses (HIV and SIV) are lentiviruses that reverse transcribe their RNA genome with subsequent integration into the genome of the target cell. How progressive infection and administration of antiretrovirals (ARVs) longitudinally influence the transcriptomic and epigenetic landscape of particular T cell subsets, and how these may influence the genetic location of integration are unclear. Here, we use RNAseq and ATACseq to study the transcriptomics and epigenetic landscape of longitudinally sampled naïve and memory CD4+ and CD8+ T cells in two species of non-human primates prior to SIV infection, during chronic SIV infection, and after administration of ARVs. We find that SIV infection leads to significant alteration to the transcriptomic profile of all T cell subsets that are only partially reversed by administration of ARVs. Epigenetic changes were more apparent in animals with longer periods of untreated SIV infection and correlated well with changes in corresponding gene expression. Known SIV integration sites did not vary due to SIV status but did contain more open chromatin in rhesus macaque memory T cells, and the expression of proteasome-related genes at the pre-SIV timepoint correlated with subsequent viremia.IMPORTANCEChronic inflammation during progressive human and simian immunodeficiency virus (HIV and SIV) infections leads to significant co-morbidities in infected individuals with significant consequences. Antiretroviral (ARV)-treated individuals also manifest increased levels of inflammation which are associated with increased mortalities. These data will help guide rational development of modalities to reduce inflammation observed in people living with HIV and suggest mechanisms underlying lentiviral integration site preferences.

Keywords: HIV; SIV; epigenetic; integration; transcriptomic.

MeSH terms

  • Animals
  • Anti-Retroviral Agents* / pharmacology
  • Anti-Retroviral Agents* / therapeutic use
  • CD4-Positive T-Lymphocytes / drug effects
  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / metabolism
  • CD8-Positive T-Lymphocytes / drug effects
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / metabolism
  • Epigenesis, Genetic* / drug effects
  • Macaca mulatta / genetics
  • Macaca mulatta / immunology
  • Macaca mulatta / virology
  • Macaca nemestrina / genetics
  • Macaca nemestrina / immunology
  • Macaca nemestrina / virology
  • Memory T Cells* / drug effects
  • Memory T Cells* / immunology
  • Memory T Cells* / metabolism
  • Memory T Cells* / virology
  • Proteasome Endopeptidase Complex / genetics
  • RNA-Seq
  • Simian Acquired Immunodeficiency Syndrome* / drug therapy
  • Simian Acquired Immunodeficiency Syndrome* / genetics
  • Simian Acquired Immunodeficiency Syndrome* / immunology
  • Simian Acquired Immunodeficiency Syndrome* / virology
  • Simian Immunodeficiency Virus* / drug effects
  • Simian Immunodeficiency Virus* / immunology
  • Transcriptome* / drug effects
  • Viremia / drug therapy
  • Viremia / genetics
  • Viremia / immunology
  • Viremia / virology

Substances

  • Anti-Retroviral Agents
  • Proteasome Endopeptidase Complex